JPGR Review

REVIEWS

Seaweed Extracts as Biostimulants of Plant Growthand Development

Wajahatullah Khan Æ Usha P. Rayirath Æ Sowmyalakshmi Subramanian ÆMundaya N. Jithesh Æ Prasanth Rayorath Æ D. Mark Hodges ÆAlan T. Critchley Æ James S. Craigie Æ Jeff Norrie ÆBalakrishan Prithiviraj

Received: 24 October 2008 / Accepted: 18 March 2009 / Published online: 8 May 2009

� Springer Science+Business Media, LLC 2009

Abstract Marine algal seaweed species are often regar-

ded as an underutilized bioresource, many have been used

as a source of food, industrial raw materials, and in ther-

apeutic and botanical applications for centuries. Moreover,

seaweed and seaweed-derived products have been widely

used as amendments in crop production systems due to the

presence of a number of plant growth-stimulating com-

pounds. However, the biostimulatory potential of many of

these products has not been fully exploited due to the lack

of scientific data on growth factors present in seaweeds and

their mode of action in affecting plant growth. This article

provides a comprehensive review of the effect of various

seaweed species and seaweed products on plant growth and

development with an emphasis on the use of this renewable

bioresource in sustainable agricultural systems.

Keywords Seaweed � Biostimulants � Plant growth �Plant development � Biotic and abiotic stresses �Plant-microbe interactions

Introduction

Seaweeds form an integral part of marine coastal ecosys-

tems. They include the macroscopic, multicellular marine

algae that commonly inhabit the coastal regions of the

world’s oceans where suitable substrata exist. It has been

estimated that there are about 9,000 species of macroalgae

broadly classified into three main groups based on their

pigmentation (for example, Phaeophyta, Rhodophyta, and

Chlorophyta; or the brown, red, and green algae, respec-

tively). Brown seaweeds are the second most abundant

group comprising about 2,000 species which reach their

maximum biomass levels on the rocky shores of the tem-

perate zones. They are the type most commonly used in

agriculture (Blunden and Gordon 1986) and, among them,

Ascophyllum nodosum (L.) Le Jolis is the most researched

(Ugarte and others 2006). Besides A. nodosum, other brown

algae such as Fucus spp., Laminaria spp., Sargassum spp.,

and Turbinaria spp. are used as biofertilizers in agriculture

(Hong and others 2007).

The benefits of seaweeds as sources of organic matter

and fertilizer nutrients have led to their use as soil condi-

tioners for centuries (Blunden and Gordon 1986; Metting

and others 1988; Temple and Bomke 1988). Some

15 million metric tonnes of seaweed products are produced

annually (FAO 2006), a considerable portion of which is

W. Khan � U. P. Rayirath � S. Subramanian �M. N. Jithesh � P. Rayorath � B. Prithiviraj (&)

Department of Plant and Animal Sciences, Nova Scotia

Agricultural College, P.O. Box 550, 58 River Road,

Truro, NS B2N 5E3, Canada

e-mail: [email protected]

D. M. Hodges

Atlantic Food and Horticulture Research Centre,

Agriculture and Agri-Food Canada, 32 Main Street,

Kentville, NS B4N 1J5, Canada

A. T. Critchley � J. S. Craigie � J. Norrie

Acadian Seaplants Limited, 30 Brown Avenue,

Dartmouth, NS B3B 1X8, Canada

J. S. Craigie

Institute for Marine Biosciences, National Research Council of

Canada, 1411 Oxford Street, Halifax, NS B3H 3Z1, Canada

Present Address:W. Khan

Department of Biochemistry, College of Science,

King Saud University, P.O. Box 2455, Riyadh 11451, Kingdom

of Saudi Arabia

123

J Plant Growth Regul (2009) 28:386–399

DOI 10.1007/s00344-009-9103-x

used for nutrient supplements and as biostimulants or

biofertilizers to increase plant growth and yield. A number

of commercial seaweed extract products are available for

use in agriculture and horticulture (Table 1).

Numerous studies have revealed a wide range of bene-

ficial effects of seaweed extract applications on plants, such

as early seed germination and establishment, improved

crop performance and yield, elevated resistance to biotic

and abiotic stress, and enhanced postharvest shelf-life of

perishable products (Beckett and van Staden 1989; Hankins

and Hockey 1990; Blunden 1991; Norrie and Keathley

2006) (Fig. 1).

Modes of Action of Growth Stimulatory Factors

in Seaweed Extracts

Seaweed products exhibit growth-stimulating activities,

and the use of seaweed formulations as biostimulants in

crop production is well established. Biostimulants are

defined as ‘‘materials, other than fertilizers, that promote

plant growth when applied in small quantities’’ and are also

referred to as ‘‘metabolic enhancers’’ (Zhang and Schmidt

1997). Seaweed components such as macro- and microel-

ement nutrients, amino acids, vitamins, cytokinins, auxins,

and abscisic acid (ABA)-like growth substances affect

cellular metabolism in treated plants leading to enhanced

growth and crop yield (Crouch and others 1992; Crouch

and van Staden 1993a; Reitz and Trumble 1996; Durand

and others 2003; Stirk and others 2003; Ordog and others

2004). Seaweed extracts are bioactive at low concentra-

tions (diluted as 1:1000 or more) (Crouch and van Staden

1993a). Although many of the various chemical compo-

nents of seaweed extracts and their modes of action remain

unknown, it is plausible that these components exhibit

synergistic activity (Fornes and others 2002; Vernieri and

others 2005).

Chemical Components of Seaweed that Affect Plant

Growth

Carbohydrates, Minerals, and Trace Elements

Seaweeds, particularly the red and brown algae, are a

source of unusual and complex polysaccharides not present

Table 1 Commercial seaweed products used in the agriculture and horticulture industries

Product name Seaweed name Company Application

Acadian� Ascophyllum nodosum Acadian Agritech Plant growth stimulant

Acid Buf Lithothamnium calcareum Chance & Hunt Limited Animal feed

Agri-Gro Ultra Ascophyllum nodosum Agri Gro Marketing Inc. Plant growth stimulant

AgroKelp Macrocystis pyrifera Algas y Bioderivados Marinos, S.A. de C.V. Plant growth stimulant

Alg-A-Mic Ascophyllum nodosum BioBizz Worldwide N.V. Plant growth stimulant

Bio-GenesisTM High TideTM Ascophyllum nodosum Green Air Products, Inc. Plant growth stimulant

Biovita Ascophyllum nodosum PI Industries Ltd Plant growth stimulant

Emerald RMA Red marine algae Dolphin Sea Vegetable Company Health product

Espoma Ascophyllum nodosum The Espoma Company Plant growth stimulant

Fartum� Unspecified Inversiones Patagonia S.A. Biofertilizer

Guarantee� Ascophyllum nodosum MaineStream Organics Plant growth stimulant

Kelp Meal Ascophyllum nodosum Acadian Seaplants Ltd Plant growth stimulant

Kelpak Ecklonia maxima BASF Plant growth stimulant

Kelpro Ascophyllum nodosum Tecniprocesos Biologicos, S.A. de C.V. Plant growth stimulant

Kelprosoil Ascophyllum nodosum Productos del Pacifico, S.A. deC.V. Plant growth stimulant

Maxicrop Ascophyllum nodosum Maxicrop USA, Inc. Plant growth stimulant

Nitrozime Ascophyllum nodosum Hydrodynamics International Inc. Plant growth stimulant

Profert� Durvillea antarctica BASF Plant biostimulant

Sea Winner Unspecified China Ocean University Product Development Co., Ltd Plant biostimulant

Seanure Unspecified Farmura Ltd. Plant growth stimulant

Seasol� Durvillea potatorum Seasol International Pty Ltd Plant growth stimulant

Soluble Seaweed Extract Ascophyllum nodosum Technaflora Plant Products, LTD Plant growth stimulant

Stimplex� Ascophyllum nodosum Acadian Agritech Plant growth stimulant

Synergy Ascophyllum nodosum Green Air Products, Inc. Plant growth stimulant

Tasco� Ascophyllum nodosum Acadian Agritech Animal feed

J Plant Growth Regul (2009) 28:386–399 387

123

in land plants (Siegel and Siegel 1973; Painter 1983;

Blunden and Gordon 1986; Craigie 1990; Chizhov and

others 1998; Duarte and others 2001) (Table 2). For

example, the brown seaweeds Ascophyllum nodosum,

Fucus vesiculosus, and Saccharina longicruris contain the

polysaccharides laminaran, fucoidan, and alginate (Painter

1983; Lane and others 2006). Laminaran is a (1,3)-b-D-

glucan with b-(1,6) branching (Nelson and Lewis 1973;

Zvyagintseva and others 1999). Although the precise

structures of fucoidans are not fully established, fucoidan

from A. nodosum consists primarily of sulfated fucose

linked in a-(1,3) and a-(1,4) configuration (Chevolot and

others 1999; Chevolot and others 2001; Daniel and others

2001; Marais and Joseleau 2001). Alginate is a block

copolymer structure composed of D-mannuronic and L-

guluronic acids with b-(1,4)-glycosidic linkages. The

properties of the various alginates differ depending on the

position of each monomeric unit in the chain, the average

molecular weight of the polymer, and the nature of its

associated counter ions. The monomers may alternate in

some regions of the alginate (heteropolymeric), or they

may occur in contiguous groups to produce homopolymeric

sections with either monomer within the alginate molecule

(Painter 1983; Rioux and others 2007). Of these three

polysaccharides, laminaran and fucoidan exhibit a wide

range of biological activities (Rioux and others 2007).

Direct effects of fucoidan on plants have not yet been

reported but sulfated fucoidans from brown algae have

evinced biological activities in mammalian systems

(McClure and others 1992; Angstwurm and others 1995;

Mauray and others 1995). Laminarin has been shown to

stimulate natural defense responses in plants and is

involved in the induction of genes encoding various path-

ogenesis–related (PR) proteins with antimicrobial proper-

ties (Fritig and others 1998; van Loon and van Strien

1999).

Growth Hormones

The concentration of mineral nutrient elements present in

commercial seaweed concentrates (SWCs) alone cannot

account for the growth responses elicited by seaweed

extracts (Blunden 1972, 1991). Beneficial effects observed

in various plant growth bioassays have led to speculation

that SWCs contain plant growth-regulatory substances

(Williams and others 1981; Tay and others 1985; Mooney

and van Staden 1986). Furthermore, the wide range of

growth responses induced by seaweed extracts implies the

presence of more than one group of plant growth-promot-

ing substances/hormones (Tay and others 1985; Crouch

and van Staden 1993a).

Cytokinins have been detected in fresh seaweeds (Hus-

sein and Boney 1969) and seaweed extracts (Brain and

others 1973). The cytokinins present in seaweed formula-

tions include trans-zeatin, trans-zeatin riboside, and dihy-

dro derivatives of these two forms (Stirk and van Staden

1997). Liquid chromatography/mass spectroscopy

(LC/MS) analysis of 31 seaweed species representing

various groups revealed that zeatin (Z) and isopentenyl (IP)

conjugates of cytokinins are the predominant cytokinins

Fig. 1 Schematic

representation of physiological

effects elicited by seaweed

extracts and possible

mechanism(s) of bioactivity

388 J Plant Growth Regul (2009) 28:386–399

123

(Stirk and others 2003). Seaweed concentrates also con-

tained aromatic cytokinins BAP (benzyl amino purine) and

topolin (6-[3-hydroxybenzyl-amino] purine) derivatives)

(Stirk and others 2004).

Marine algae are also reportedly rich in auxins and

auxin-like compounds (Crouch and van Staden 1993a). An

A. nodosum extract had as high as 50 mg IAA (indole

acetic acid) per gram of dry extract (Kingman and Moore

1982). Similarly, an extract of Ecklonia maxima exhibited

a remarkable root-promoting activity on mung bean, an

effect reminiscent of auxins (Crouch and van Staden 1991).

Gas chromatography/mass spectroscopy (GC/MS) analysis

of the extract revealed the presence of indole compounds,

including IAA in SWC (Crouch and others 1992).

Auxins have been detected in other algal species like

Porphyra perforata, but the levels found were low (Zhang

and others 1993). In higher plants IAA occurs as an inac-

tive conjugate with carboxyl groups, glycans, amino acids,

and peptides, which, upon hydrolysis, are converted to free

active IAA (Bartel 1997). Stirk and others (2004) found

four amino acid and three indole conjugates of IAA in the

extracts of two seaweeds, E. maxima and Macrocystis

pyrifera. Biologically active auxin-like compounds other

than IAA were reported in alkaline hydrolyzates of

A. nodosum, Fucus vesiculosus, and other seaweeds

(Buggeln and Craigie 1971).

The water-soluble growth inhibitors extracted from

Laminaria digitata and A. nodosum resulted in marked

inhibition of lettuce hypocotyl growth (Hussain and Boney

1973). One of these substances seemed to be similar to

ABA as revealed by bioassay, thin-layer, and gas-liquid

chromatography analysis. Presence of ABA in seaweeds

has also been reported by others such Tietz and others

(1989) (green algae) and Kingman and Moore (1982)

(A. nodosum).

Betaines

Ascophyllum nodosum extracts contain various betaines

and betaine-like compounds (Blunden and others 1986). In

plants, betaines serve as a compatible solute that alleviates

osmotic stress induced by salinity and drought stress;

however, other roles have also been suggested (Blunden

and Gordon 1986), such as enhancing leaf chlorophyll

content of plants following their treatment with seaweed

extracts (Blunden and others 1997). This increase in

chlorophyll content may be due to a decrease in chloro-

phyll degradation (Whapham and others 1993). Yield

enhancement effects due to improved chlorophyll content

in leaves of various crop plants have been attributed to the

betaines present in the seaweed (Genard and others 1991;

Whapham and others 1993; Blunden and others 1997). It

has been indicated that betaine may work as a nitrogen

source when provided in low concentration and serve as an

osmolyte at higher concentrations (Naidu and others 1987).

Betaines have been shown to play a part in successful

formation of somatic embryos from cotyledonary tissues

and mature seeds of tea (Wachira and Ogada 1995; Akula

and others 2000).

Sterols

As with many other eukaryotic cells, sterols are an essen-

tial group of lipids. Generally, a plant cell contains a

mixture of sterols, such as b-sitosterol, stigmasterol,

24-methylenecholesterol, and cholesterol (Nabil and Cos-

son 1996). Brown seaweed chiefly contains fucosterol and

fucosterol derivatives, whereas red seaweeds primarily

contain cholesterol and cholesterol derivatives. Green

seaweed accumulates mainly ergosterol and 24-methylen-

echolesterol (Ragan and Chapman 1978; Hamdy and

Dawes 1988; Govindan and others 1993; Nabil and Cosson

1996) (Table 3).

Table 2 Selected polysaccharide constituents of green, red, and

brown seaweeds

Seaweed Polysaccharides

Chlorophyceae

(Green)

Amylose, amylopectin

Cellulose

Complex hemicellulose

Glucomannans

Mannans

Inulin

Laminaran

Pectin

Sulfated mucilages

(glucuronoxylorhamnans)

Xylans

Rhodophyceae (Red) Agars, agaroids

Carrageenans

Cellulose

Complex mucilages

Furcellaran

Glycogen (floridean starch)

Mannans

Xylans, rhodymenan

Phaeophyceae

(Brown)

Alginates

Cellulose

Complex sulfated heteroglucans

Fucose containing glycans

Fucoidans

Glucuronoxylofucans

Laminarans

Lichenan-like glucan


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Effect on Soil Health

Soil Structure and Moisture Retention

Besides eliciting a growth-promoting effect on plants,

seaweeds also affect the physical, chemical, and bio-

logical properties of soil which in turn influence plant

growth. Seaweeds and seaweed extracts enhance soil

health by improving moisture-holding capacity and by

promoting the growth of beneficial soil microbes.

Brown seaweeds are rich in polyuronides such as algi-

nates and fucoidans. The gelling and chelating abilities

of these polysaccharides coupled with their hydrophilic

properties make these compounds important in food

processing and in the agricultural and pharmaceutical

industries (Cardozo and others 2007). Alginate occurs

in the cell walls of seaweeds as a mixed salt with the

major cations being Na, Ca, Mg, and K together with a

number of minor metal counterions. The molecular

mass of alginate isolated from A. nodosum, F. vesicu-

losus, and S. longicruris varies between 106.6 and

177.3 kDa (Rioux and others 2007). Alginates possess

unique and valuable properties attributable to the

varying proportions of their two monomeric units

(D-mannuronic acid and L-guluronic acid) that are

arranged in block copolymer structures. The free acid

form, alginic acid, is insoluble in water, as are alginates

of certain divalent and polyvalent metal ions. Knowl-

edge of these properties together with that of chain

lengths and copolymer composition are used to control

the gel structure and porosity of alginates for agricul-

tural, pharmaceutical, and industrial uses (Lewis and

others 1988; Skjak-Braek and others 1989). For exam-

ple, alginates are widely used in formulating slow-

release pharmaceuticals (Kim and others 2005; Chan

and Heng 2002; Wong and others 2002) and pesticides

(Vollner 1990; Davis and others 1996; Gonzalez-Pradas

and others 1999; Kumbar and others 2003). The wide-

spread interest in alginate is due in part to its biode-

gradable nature and the relatively non toxic nature of

this natural compound.

Salts of alginic acid combine with the metallic ions in

the soil to form high-molecular-weight complexes that

absorb moisture, swell, retain soil moisture, and improve

crumb structure. This results in better soil aeration and

capillary activity of soil pores which in turn stimulate

the growth of the plant root system as well as boost soil

microbial activity (Eyras and others 1998; Gandhiyappan

and Perumal 2001; Moore 2004). The polyanionic

properties of seaweeds and unicellular algae have proved

valuable in remediation of soils, especially those con-

taminated with heavy metals (Metting and others 1988;

Blunden 1991).

Table 3 Common sterol constituents of green, red, and brown

seaweeds

Seaweed Type of sterol

Chlorophyceae (Green) 22-Dehydrocholesterol

24-Methylenecholesterol

24-Methylenecycloartanol

28-Isofucosterol

Brassicasterol

Cholesterol

Clerosterol

Clionasterol

Codisterol

Cycloartannol

Cycloartenol

Decortinol

Decortinone

Ergosterol

Fucosterol

Isodecortinol

Ostreasterol

ß-Stitosterol

Zymosterol

Chondrillasterol

D5 - Ergostenol

D7 - Ergostenol

Poriferastenol

24-Methylenophenol

Rhodophyceae (Red) 22-Dehydrocholesterol


Campesterol

Cholesterol

Cycloartenol

Desmosterol

Fucosterol

Stigmasterol

Brassicasterol

5-Dihydroergosterol

D5 - Ergostenol

Obusifoliol

D4,5 - Ketosteroids

Sitosterol

Phaeophyceae (Brown) 22-Dehydrocholesterol

Cycloartenol

24-Methylenecycloartenol


Fucosterol

Cholesterol

Campesterol

Stigmasterol

Brassicasterol

Clionasterol

Porifasterol


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Effect on Rhizosphere Microbes

Application of seaweeds and seaweed extracts triggers the

growth of beneficial soil microbes and secretion of soil-

conditioning substances by these microbes. As mentioned,

alginates affect soil properties and encourage growth of

beneficial fungi. Ishii and others (2000) observed that

alginate oligosaccharides, produced by enzymatic degra-

dation of alginic acid mainly extracted from brown algae,

significantly stimulated hyphal growth and elongation of

arbuscular mycorrhizal (AM) fungi and triggered their

infectivity on trifoliate orange seedlings. Extracts of vari-

ous marine brown algae [Laminaria japonica Areschoug

and Undaria pinnatifida (Harvey) Suringar] could be used

as an AM fungus growth promoter (Kuwada and others

2006). Kuwada and others (1999) previously showed that

methanol extracts of brown algae fractionated by flash

chromatography promoted in vitro AM hyphal growth as

well as improved root colonization by AM fungi on trifo-

liate orange, Poncirus trifoliate (Linn.) Raf., seedlings.

Indigenous AM fungi demonstrated a 27% improvement in

root colonization, while spore number was increased about

21% over the controls when liquid fertilizer containing

tangle (L. japonica) extracts was applied via a sprinkler

system in a citrus orchard (Kuwada and others 2000).

Kuwada and others (2006) reported that organic fractions

(25% MeOH eluates) of red and green algae considerably

improved in vitro hyphal growth of AM fungi. Their results

showed that application of the 25% MeOH eluates of red

and green algal extracts to roots of papaya (Carica papaya

Linn.) and passion fruit (Passiflora edulis Sims.) improved

mycorrhizal development more than the control treatment.

Kuwada and others (2006) implied that both red and green

algae have AM stimulatory compounds which play a part

in mycorrhizal development in higher plants.

Limited research has been conducted on the effects of

seaweed extracts on other beneficial AM fungi.

Effect on Plant Growth and Health

Root Development and Mineral Absorption

Seaweed products promote root growth and development

(Metting and others 1990; Jeannin and others 1991). The

root-growth stimulatory effect was more pronounced when

extracts were applied at an early growth stage in maize, and

the response was similar to that of auxin, an important root-

growth-promoting hormone (Jeannin and others 1991).

SWC applications reduce transplant shock in seedlings of

marigold, cabbage (Aldworth and van Staden 1987), and

tomato (Crouch and van Staden 1992) by increasing root

size and vigor. SWC treatment enhanced both root:shoot

ratios and biomass accumulation in tomato seedlings by

stimulating root growth (Crouch and van Staden 1992).

Similarly, wheat plants treated with SWC Kelpak�

(Table 3) exhibited an increase in root:shoot dry mass

ratio, indicating that the components in the seaweed had a

considerable effect on root development (Nelson and van

Staden 1986). This stimulatory activity was lost on ashing,

suggesting that the active principles in the seaweed extract

were organic in nature (Finnie and van Staden 1985). The

root-growth-promoting activity was observed when the

seaweed extracts were applied either to the roots or as a

foliar spray (Biddington and Dearman 1983; Finnie and

van Staden 1985). The concentration of kelp extract is a

critical factor in its effectiveness as Finnie and van Staden

(1985) showed for tomato plants in which high concen-

trations (1:100 seaweed extract:water) inhibited root

growth but stimulatory effects were found at a lower

concentration (1:600). Biostimulants in general are capable

of affecting root development by both improving lateral

root formation (Atzmon and van Staden 1994; Vernieri and

others 2005) and increasing total volume of the root system

(Thompson 2004; Slavik 2005; Mancuso and others 2006).

An improved root system could be influenced by

endogenous auxins as well as other compounds in the

extracts (Crouch and others 1992). Seaweed extracts

improve nutrient uptake by roots (Crouch and others 1990),

resulting in root systems with improved water and nutrient

efficiency, thereby causing enhanced general plant growth

and vigor.

Effect on Shoot Growth and Photosynthesis

Seaweeds and seaweed products enhance plant chlorophyll

content (Blunden and others 1997). Application of a low

concentration of Ascophyllum nodosum extract to soil or on

foliage of tomatoes produced leaves with higher chlorophyll

content than those of untreated controls. This increase in

chlorophyll content was a result of reduction in chlorophyll

degradation, which might be caused in part by betaines in the

seaweed extract (Whapham and others 1993). Glycine

betaine delays the loss of photosynthetic activity by inhib-

iting chlorophyll degradation during storage conditions in

isolated chloroplasts (Genard and others 1991).

In a recent study (Rayorath and others 2008), extracts of

A. nodosum have been shown to affect the root growth of

Arabidopsis at very low concentrations (0.1 g L-1),

whereas plant height and number of leaves were affected at

concentrations of 1 g L-1. Plants treated with extracts

showed growth enhancement effects over control plants;

for example, plants treated with A. nodosum extract were at

a more advanced developmental stage when compared with

untreated plants and the effect was concentration depen-

dent (Fig. 2; unpublished results).


123

Although they may contain different levels of minerals,

biostimulants are unable to provide all the nutrients needed

by a plant in required quantities (Schmidt and others 2003);

however, their main benefit is to improve plant mineral

uptake by the roots (Vernieri and others 2005) and in the

leaves (Mancuso and others 2006).

Effect on Crop Yield

Seaweed concentrate triggers early flowering and fruit set

in a number of crop plants (Abetz and Young 1983;

Featonby-Smith and van Staden 1987; Arthur and others

2003). For example, tomato seedlings treated with SWC set

more flowers earlier than the control plants and this was not

considered to be a stress response (Crouch and van Staden

1992). In many crops yield is associated with the number of

flowers at maturity. As the onset and development of

flowering and the number of flowers produced are linked to

the developmental stage of plants, seaweed extracts prob-

ably encourage flowering by initiating robust plant growth.

Yield increases in seaweed-treated plants are thought to be

associated with the hormonal substances present in the

extracts, especially cytokinins (Featonby-Smith and van

Staden 1983a, b, 1984). Cytokinins in vegetative plant

organs are associated with nutrient partitioning, whereas in

reproductive organs, high levels of cytokinins may be

linked with nutrient mobilization. Fruit ripening generally

causes an increase in transport of nutrient resources within

the developing plant (Hutton and van Staden 1984, Adams-

Phillips and others 2004) and the fruits have the capacity to

serve as strong sinks for nutrients (Varga and Bruinsma

1974; Adams-Phillips and others 2004). Photosynthate

distribution could be shifted, perhaps markedly, moving

from vegetative parts (roots, stem, and young leaves) to the

developing fruit, to be utilized in fruit development

(Nooden and Leopold 1978). Fruit treated with seaweed

extracts had higher concentrations of cytokinins compared

to untreated fruit in tomato (Featonby-Smith and van Sta-

den 1984). Cytokinins have been implicated in nutrient

mobilization in vegetative plant organs (Gersani and Kende

1982) as well as reproductive organs (Davey and van

Staden 1978). Such a response indicates that seaweed

extracts are involved either in enhancing the mobilization

of cytokinins from the roots to the developing fruit, or,

more likely, by improving the amount or synthesis of

endogenous fruit cytokinins (Hahn and others 1974).

Higher root cytokinin levels have also been found in sea-

weed extract-treated plants (Featonby-Smith 1984). This

increase in cytokinin availability will eventually result in a

greater supply of cytokinins to the maturing fruit. Devel-

oping fruits and seeds demonstrated increased endogenous

cytokinin levels (Crane 1964; Nitsch 1970; Letham 1994).

It has been reported that the increased cytokinin concen-

tration is associated with translocation of cytokinin from

roots to other plant parts (Stevens and Westwood 1984;

Carlson and others 1987).

Seaweed extract increased fruit yield when sprayed on

tomato plants during the vegetative stage, producing large-

sized fruits (30% increase in fresh fruit weight over the

controls) with superior quality (Crouch and van Staden

1992). The number of flowers and seeds per flower head

increased (as much as 50% over the control) (van Staden

and others 1994) when marigold seedlings were treated

with SWC Kelpak immediately after transplanting (Ald-

worth and van Staden 1987). Application of Maxicrop�

enhanced harvestable yield in lettuce, whereas an increase

in the heart size of the florets and curd diameter was

observed in cauliflower (Abetz and Young 1983). Simi-

larly, a substantial increase in yield was achieved in barley

(Featon-Smith and van Staden 1987) and peppers (Arthur

and others 2003) after treatment with Kelpak.

Foliar application of seaweed liquid extract (Kelpak 66)

enhanced bean yield by 24% (Nelson and van Staden

1984). Kelpak 66 also had a similar effect on the yield of

wheat under potassium stress, although its application had

no significant effect on the plants receiving an adequate K

supplement (Beckett and van Staden 1989). Norrie and

Keathley (2006) have reported that A. nodosum extracts

showed positive effects on the yield of ‘Thompson seed-

less’ grape (Vitis vinifera L.) consistently over a 3-year

period. They observed that the A. nodosum-treated plants

always outperformed (in terms of berries per bunch, berry

size, berry weight, rachis length, and the number of pri-

mary bunches per plant) the controls maintained under the

regular crop management program, and resulted in

improved fruit size (13% increase), weight (39% increase),

and yields (60.4% increase over the control).

Vegetative Propagation

Seaweed products are exploited in conventional vegetative

propagation in many crop species (Crouch and van Staden

1991; Atzmon and van Staden 1994; Kowalski and others

1999). It is common practice to apply auxins exogenously

to enhance rooting in cuttings in certain species that are

difficult to root. It has been observed that treating cuttings

Fig. 2 Arabidopsis thaliana plants treated with different A. nodosumextracts (1 g L-1) showed growth enhancement effects over the

control plants 3 weeks after treatment


123

of some flowering plants like marigold (Tagetus patula) for

about 18 h with 10% SWC Kelpak increased the number

and dry weight of roots (Crouch and van Staden 1991).

Similarly, Kelpak, when applied at a 1:100 dilution,

increased the number of rooted cuttings and improved the

vigor of the roots in difficult-to-root cuttings of Pinus pinea

(Atzmon and van Staden 1994). In another study, Leclerc

and others (2006) observed that foliar application of

commercial liquid seaweed extract from Ascophyllum

nodosum (Acadian Seaplants Limited), supplemented with

BA and IBA, enhanced the number of propagules (crown

divisions) per plant in the ornamental herbaceous perennial

Hemerocallis sp.

Resistance to Environmental Stresses

Effects of SWCs in Alleviating Abiotic Stress in Crop

Plants

Abiotic stresses such as drought, salinity, and temperature

extremes can reduce the yield of major crops (Wang and

others 2003) and limit agricultural production worldwide.

For example, salinity and drought are becoming wide-

spread in many regions of the world, with an estimated

50% of all arable lands possibly being salinized by 2050

(Flowers and Yeo 1995). Many abiotic factors such as

drought, salinity, and temperature are manifested as

osmotic stress and cause secondary effects like oxidative

stress, leading to an accumulation of reactive oxygen

species (ROS) such as the superoxide anion (O2• -) and

hydrogen peroxide (H2O2) (Mittler 2002). These are known

to damage DNA, lipids, carbohydrates, and proteins and

also cause aberrant cell signaling (Arora and others 2002).

Seaweed extracts from Ascophyllum nodosum have been

shown to contain betaines, including gamma-aminobutyric

acid betaine, 6-aminovaleric acid betaine, and glycine

betaine (Blunden and others 1986). To test whether the

increased chlorophyll content in leaves caused by seaweed

extract treatment may be due in part to the betaines present

in the extract, the effects of Algifert 25, an alkaline extract

of A. nodosum, were compared with those of a mixture of

known betaine constituents of A. nodosum (Blunden and

others 1997). Blunden and others (1986) used a betaine

mixture in the same concentrations as those present in

the diluted seaweed extract (gamma-aminobutyric

acid betaine, 0.96 mg L-1; 6-aminovaleric acid betaine,

0.43 mg L-1; glycine betaine, 0.34 mg L-l). Results

showed that similar leaf chlorophyll levels were recorded

in both seaweed- and betaine-treated plants. Sixty-three

and 69 days after application of SWC, leaf chlorophyll

contents, as expressed in SPAD (soil-plant analysis

development; Minolta Corporation, Japan) units, were

27.70 and 26.48, respectively, for seaweed extract and

27.30 and 23.60, respectively, for the betaine treatment.

Both treatments resulted in higher chlorophyll levels versus

controls measured on both days. The results imply that the

enhanced leaf chlorophyll content of plants treated with

SWC might depend on betaines present in the extract

(Blunden and others 1997).

Plants sprayed with seaweed extracts also exhibit

enhanced salt and freezing tolerance (Mancuso and others

2006). Commercial formulations of Ascophyllum extracts

(Seasol�) improved freezing tolerance in grapes. Grape-

vines sprayed with Seasol (0.8%) showed a reduction in

leaf osmotic potential, a key indicator of osmotic tolerance.

The treated plants showed an average osmotic potential of

-1.57 MPa after 9 days of seaweed extract treatment,

whereas it was -1.51 MPa in untreated controls (Wilson

2001). Field studies on winter barley (Hordeum vulgare cv

Igri) have shown that application of seaweed extract

(Maxicrop) improves winter hardiness and increases frost

resistance (Burchett and others 1998).

Taken collectively, these studies suggest that seaweed

products elicit abiotic stress tolerance in plants and that the

bioactive substances derived from seaweeds impart stress

tolerance and enhance plant performance. The chemistry of

bioactive compounds in the seaweed and the physiologic

mechanism of action of the compounds that impart this

tolerance are largely unknown. However, a number of

reports suggest that the beneficial antistress effects of

seaweed extracts may be related to cytokinin activity. For

example, Zhang and Ervin (2004) conducted experiments

to confirm the action of seaweed extracts (Ascophyllum

nodosum) on drought tolerance in creeping bentgrass.

Drought-stressed plants treated with a combination of

humic acid and seaweed extract had root mass enhanced by

21–68%, foliar tocopherol by 110%, and endogenous

zeatin riboside (ZR) by 38%. A systematic analysis of

cytokinins, namely, ZR and isopentenyl adenosine (iPA),

was then performed on A. nodosum extract using enzyme-

linked immunosorbent assay (ELISA). Seaweed extract

contained substantial amounts of cytokinins amounting to

66 lg g-1 as zeatin riboside. Ashing of the seaweed extract

reduced the effectiveness of the treatments suggesting the

organic nature of the bioactive compound (Zhang and Er-

vin 2004). Cytokinins mitigate stress-induced free radicals

by direct scavenging and by preventing reactive oxygen

species (ROS) formation by inhibiting xanthine oxidation

(McKersie and Leshem 1994; Fike and others 2001). It was

hypothesized that seaweed extract-induced heat tolerance

in creeping bent grass might be attributed largely to the

cytokinin components in the seaweed extracts (Ervin and

others 2004; Zhang and Ervin 2008). However, it has also

been reported that Kelpak seems to mediate stress tolerance

by enhancing K? uptake, although synthetic


123

benzylaminopurine (BA), at a similar concentration to

natural cytokinin present in Kelpak, showed no effect on

yield, irrespective of the K? supply. Hence, the beneficial

effects of seaweed extract against abiotic stress could also

be partly elicited by bioactive chemicals other than cyto-

kinin (Beckett and van Staden 1989).

Reactive oxygen species (ROS) are a common factor in

many abiotic stresses such as salinity, ozone exposure, UV

irradiation, temperature extremes, and drought (Hodges

2001). Application of an A. nodosum extract (Tasco�) to

unstressed turf grasses increased the activity of the anti-

oxidant enzyme superoxide dismutase (SOD), which

scavenges superoxide (Fike and others 2001). In another

study, tall fescue (Festuca arundinacea) treated with 0, 1.7,

or 3.4 kg ha_1 of A. nodosum extract exhibited increased

SOD activity in all 3 years of the study by an average of

approximately 30% (Zhang 1997). Similarly, Ayad (1998)

reported an increase in SOD, glutathione reductase (GR),

and ascorbate peroxidase (AsPX) activities in genetically

similar endophyte-infected and endophyte-free tall fescue

in response to 3.4 kg Tasco ha-1. Thus, the primary effect

of Tasco application to tall fescue in these experiments

seems to be through an increase in antioxidant capacity

(Fike and others 2001).

Effect of SWC in Alleviating Biotic Stress

Seaweed extracts have been shown to enhance plant

defense against pest and diseases (Allen and others 2001).

Besides influencing the physiology and metabolism of

plants, seaweed products promote plant health by affecting

the rhizosphere microbial community.

Nematodes Seaweed extracts were found to have an

impact on the population of nematodes in the soil (Wu and

others 1997). Plants treated with seaweed extracts caused a

reduction in nematode infestation (Featonby-Smith and van

Staden 1983a; Wu and others 1997). Root knot nematode

infestation in tomato was reduced in soil amended with

commercial seaweed extracts from Ecklonia maxima (Feat-

onby-Smith and van Staden 1983a; Crouch and van Staden

1993b). Interestingly, seaweed extract treatment did not

affect the nematode population in the rhizosphere (Featonby-

Smith and van Staden 1983a) and did not show a direct

nematicidal effect. Taken together, these results suggest that

seaweed extract imparts nematode resistance possibly by

altering the auxin:cytokinin ratio in the plant. An in vitro

experiment in which excised maize roots were treated with

seaweed extract showed reduction in the reproduction of the

nematode Pratylenchus zeae by 47–63%. However, in a pot

experiment, the reproduction of P. zeae was not influenced

by seaweed extracts (De Waele and others 1988).

Fungal and bacterial pathogens Marine algae can serve

as an important source of plant defense elicitors (Cluzet and

others 2004). Plants protect themselves against pathogen

invasion by the perception of signal molecules called elici-

tors which include a wide variety of molecules such as oligo-

and polysaccharides, peptides, proteins, and lipids, often

found in the cell wall of attacking pathogens (Boller 1995;

Cote and others 1998). A variety of polysaccharides present

in algal extracts include effective elicitors of plant defense

against plant diseases (Kloareg and Quatrano 1988).

Although red algae typically contain agars and carrageenans

in their cell walls, extracts of brown algae contain alginates,

laminarans, sulfated fucans, and other complex mucilages,

and green algae (e.g., Ulva spp.) contain mucilages com-

posed of units such as rhamnose, uronic acid, and xylose

(Cluzet and others 2004). Laminaran, a linear b-(1,3)-glu-

can, and sulfated fucans from brown algae elicit multiple

defense responses in alfalfa and tobacco (Kobayashi and

others 1993; Klarzynski and others 2000, 2003). Similarly,

carrageenans, a family of sulfated linear galactans, are

effective elicitors of defense in tobacco plants (Mercier and

others 2001). Foliar sprays of A. nodosum extract reduced

Phytophthora capsici infection in Capsicum and Plasmo-

para viticola in grape (Lizzy and others 1998). Soil appli-

cation of liquid seaweed extracts to cabbage stimulated the

growth and activity of microbes that were antagonistic to

Pythium ultimum, a serious fungal pathogen that causes

damping-off disease of seedlings (Dixon and Walsh 2002).

Seaweeds are a rich source of antioxidant polyphenols with

bactericidal properties (Zhang and others 2006). The

application of A. nodosum extract and humic acid to bent-

grass (Agrostis stolonifera) increased SOD activity, which

in turn significantly decreased dollar spot disease caused by

Sclerotinia homoeocarpa.

A study using extracts of Ulva spp. against Colletotri-

chum trifolii in Medicago truncatula showed disease

resistance without the elicitation of necrotic lesions (Cluzet

and others 2004). Ulva extract elicited the expression of the

PR-10 gene. The PR-10 gene belongs to the group of

pathogenesis-related genes (PR) important for active

defense against diseases following pathogen attack (van

Loon and others 2006). Treatment of alfalfa with the algal

extracts prior to pathogen challenge resulted in an

increased resistance to Colletotrichum. cDNA array

revealed that the algal extract caused upregulation of 152

genes, mostly plant defense genes such as those involved in

phytoalexin, PR proteins, cell wall proteins, and oxylipin

pathways (Cluzet and others 2004).

Bacterial quorum sensing and effect of seaweed on

quorum sensing Quorum sensing (QS) is a communication

mechanism used by bacterial populations that are depen-

dent on cell density which, in turn, triggers and controls

gene expression that regulates various physiologic func-

tions and responses (Brelles-Marino and Bedmar 2001;

Winzer and Williams 2001; Dong and Zhang 2005). This


123

response is mediated by low-molecular-weight signal

molecules called acylated-homoserine lactones (acyl-

HSL).

The virulence of pathogenic bacteria is under the control

of the QS system. Agents that affect the QS system can

potentially alter pathogenicity. The marine red alga Delisea

pulchra synthesizes halogenated furanones and enones that

are homologous to acyl-HSL. They bind to the LuxR in the

acyl-HSL binding site and prevent the binding of acyl-HSL

autoinducers, thereby inhibiting the process of QS. These

furanones in nature seem to interfere with QS in marine

bacteria such as Serratia liquefaciens, Vibrio fischeri, and

Vibrio harveyi (Rasmussen and others 2000; Manefield and

others 2002).

Other pests Aphids and other sap-feeding insects gen-

erally avoid plants treated with seaweed extracts (Ste-

phenson 1966; Hankins and Hockey 1990). Hydrolyzed

seaweed extracts sprayed onto apple trees reduced red

spider mite populations (Stephenson 1966), and 2–3 years

of seaweed extract application resulted in a level of control

similar to that of acaricides (Stephenson 1966). Futher-

more, it was observed that the use of Maxicrop on straw-

berry plants (Fragaria sp.) greatly reduced the two-spotted

red spider mite (Tetranychus urticae) population (Hankins

and Hockey 1990). It has been suggested that seaweed

extracts might contain chelated metals that have been

shown to reduce the population of red spider mites (Ter-

riere and Rajadhyaksha 1964; Abetz 1980).

Conclusions and Future Perspectives

Seaweeds and seaweed products are increasingly used in

crop production. However, the mechanism(s) of actions of

seaweed extract-elicited physiological responses are lar-

gely unknown. As genomes of a number of plants are now

completely sequenced or nearing completion, it is possible

to look at the effects of seaweed extracts and components

of the seaweeds on the whole genome/transcriptome of

plants to better understand the mechanisms of action of

seaweed-induced growth response and stress alleviation.

For example, the use of model plants Arabidopsis thaliana

and Medicago truncatula could potentially unravel the

molecular mechanism(s) of action of seaweed extracts

(Rayorath and others 2008). The recent challenges to food

production due to the increasing occurrence of biotic and

abiotic stresses is likely due to climate change and will

further reduce yields and/or will have an impact on crops in

the 21st century (IPCC 2007). Therefore, research into

developing sustainable methods to alleviate these stresses

should be a priority. Recent studies have shown that sea-

weed extracts protect plants against a number of biotic and

abiotic stresses and offers potential for field application.

Further, seaweed extracts are considered an organic farm

input as they are environmentally benign and safe for the

health of animals and humans.

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